A Putative Mechanism for Magnetoreception by Electromagnetic Induction in the Pigeon Inner Ear

Total Page:16

File Type:pdf, Size:1020Kb

A Putative Mechanism for Magnetoreception by Electromagnetic Induction in the Pigeon Inner Ear Report A Putative Mechanism for Magnetoreception by Electromagnetic Induction in the Pigeon Inner Ear Graphical Abstract Authors Simon Nimpf, Gregory Charles Nordmann, Daniel Kagerbauer, ..., Martin Colombini, Matthew J. Mason, David Anthony Keays Correspondence [email protected] In Brief Nimpf, Nordmann et al. confirm that magnetic stimuli result in neuronal activity in the vestibular nuclei of pigeons. Hypothesizing that this is attributable to electromagnetic induction within semicircular canals of the inner ear, they demonstrate the presence of known electrosensory molecules in vestibular hair cells. Highlights d Magnetic stimuli activate neurons in the caudal vestibular nuclei d Magnetic stimuli induce a voltage in a model of a semicircular canal d Electroreceptive molecules are expressed in vestibular hair cells d We postulate that pigeons detect magnetic fields by electromagnetic induction Nimpf et al., 2019, Current Biology 29, 4052–4059 December 2, 2019 ª 2019 The Author(s). Published by Elsevier Ltd. https://doi.org/10.1016/j.cub.2019.09.048 Current Biology Report A Putative Mechanism for Magnetoreception by Electromagnetic Induction in the Pigeon Inner Ear Simon Nimpf,1,5 Gregory Charles Nordmann,1,5 Daniel Kagerbauer,2 Erich Pascal Malkemper,1 Lukas Landler,1 Artemis Papadaki-Anastasopoulou,1 Lyubov Ushakova,1 Andrea Wenninger-Weinzierl,1 Maria Novatchkova,1 Peter Vincent,3 Thomas Lendl,1 Martin Colombini,1 Matthew J. Mason,4 and David Anthony Keays1,6,* 1Research Institute of Molecular Pathology (IMP), Vienna Biocenter (VBC), Campus-Vienna-Biocenter 1, 1030 Vienna, Austria 2Atominstitut, TU Wien, Stadionallee 2, 1020 Vienna, Austria 3Department of Neurology, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06520, USA 4Department of Physiology, Development and Neuroscience, University of Cambridge, Downing Street, Cambridge CB2 3EG, UK 5These authors contributed equally 6Lead Contact *Correspondence: [email protected] https://doi.org/10.1016/j.cub.2019.09.048 SUMMARY activation in the vestibular nuclei of pigeons [5]. To perform this experiment within the laboratory environment, we built a A diverse array of vertebrate species employs the room constructed of mu metal surrounded by an aluminum Earth’s magnetic field to assist navigation. Despite Faraday cage to shield against static and oscillating magnetic compelling behavioral evidence that a magnetic fields (Figure 1A). This setup allowed us to perform experiments sense exists, the location of the primary sensory cells in a controlled, magnetically clean environment [7]. Magnetic and the underlying molecular mechanisms remain un- fields were generated using a double-wrapped, custom-built known [1]. To date, most research has focused on a 3D Helmholtz coil system situated in the center of the shielded room (Figure 1B). To reduce movement during the experiments, light-dependent radical-pair-based concept and a birds were head fixed using a surgically implanted plastic head system that is proposed to rely on biogenic magnetite post, and the body was immobilized using a 3D printed harness (Fe3O4)[2, 3]. Here, we explore an overlooked hypoth- (Figure 1C). We applied the same stimulus as Wu and Dickman, esis that predicts that animals detect magnetic fields exposing adult pigeons to a 150-mT, rotating magnetic field (n = by electromagnetic induction within the semicircular 22) or to a zero magnetic field (n = 23) for 72 min (Figures 1D–1F) canals of the inner ear [4]. Employing an assay that re- [5]. We performed this experiment both in darkness (n = 30) and lies on the neuronal activity marker C-FOS, we under broad-spectrum white light (n = 15). Birds were then confirm that magnetic exposure results in activation perfused, the brains were sliced, and matched sections contain- of the caudal vestibular nuclei in pigeons that is inde- ing the vestibular nuclei (3 sections per bird) were stained with pendent of light [5]. We show experimentally and by sera against the neuronal activity marker C-FOS. To minimize physical calculations that magnetic stimulation can variation, all staining was performed simultaneously, all slides were scanned with the same exposure settings, and C-FOS- induce electric fields in the pigeon semicircular canals positive neurons were counted using a machine-learning-based that are within the physiological range of known elec- algorithm. Using established anatomical coordinates, we troreceptive systems. Drawing on this finding, we segmented the medial vestibular nuclei (VeM) and compared report the presence of a splice isoform of a voltage- the density of C-FOS-positive cells of the experimental groups gated calcium channel (CaV1.3) in the pigeon inner [8]. We observed an increase in the density of C-FOS-positive ear that has been shown to mediate electroreception cells in both the light and dark when exposing birds to magnetic in skates and sharks [6]. We propose that pigeons fields. In the light, the average density in controls was 35.32 ± detect magnetic fields by electromagnetic induction 10.20 cells/mm2 (n = 8; mean ± SD) whereas with the magnetic 2 within the semicircular canals that is dependent on treatment it was 44.38 ± 5.72 cells/mm (n = 7; mean ± SD). In the dark, the average density for control birds was 34.70 ± the presence of apically located voltage-gated cation 2 channels in a population of electrosensory hair cells. 10.82 cells/mm (n = 15; mean ± SD) whereas with the magnetic treatment it was 50.52 ± 27.34 cells/mm2 (n = 15; mean ± SD). An application of a two-way ANOVA revealed a significant RESULTS effect of the magnetic treatment but no interaction between magnetic treatment and lighting conditions (two-way ANOVA; Magnetically Induced Activation in the Pigeon magnetic: p = 0.0176, F = 6.125; magnetic by light: p = 0.5675, Vestibular Brainstem F = 0.332) (Figures 2A and 2B; Table S1). To explore this in We set out to replicate a previous study conducted by Wu and more detail, we employed our spot-detection algorithm coupled Dickman, who reported that magnetic stimuli induce neuronal to an elastic registration to generate heatmaps showing regional 4052 Current Biology 29, 4052–4059, December 2, 2019 ª 2019 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). Figure 1. Experimental Setup for the Magnetic Activation Study (A) The magnetic activation experiments were performed inside a magnetically shielded room consisting of a Faraday cage to shield from broadband anthro- pogenic magnetic noise and a mu-metal cage to shield from the geomagnetic field. (B and C) Pigeons were placed in the center of a double-wrapped 3D Helmholtz coil system (B) located in the magnetically shielded room and immobilized by head fixation and a molded body harness (C). (D–F) Schematic illustration of the magnetic stimulus used in this study. The magnetic field vector was rotated 360 within a plane by 6 steps every 2 s (D). After each rotation the plane was shifted by 15 (E) and the procedure was repeated until a full rotation around each axis was achieved (12 planes per x, y, and z axis, respectively) (F). differences in the density of C-FOS-positive cells. This revealed nanovoltmeter (forming a loop with a diameter of 21 cm), placed an enrichment of activated neurons in the dorsomedial part of in the center of our magnetic coil system, and exposed to the the VeM in animals exposed to magnetic stimuli (Figure 2C). Pre- same rotating magnetic stimulus applied to our birds (i.e., vious tracing experiments have shown that the dorsomedial VeM 150 mT rotating 360 with 6-step changes every 2 s). We is innervated by projections from both the semicircular canals observed discrete voltage spikes when the magnetic field stim- and the otolith organs located in the inner ear [9]. ulus was presented and with each stepwise change (Figure 3B). In accordance with Faraday’s law of electromagnetic induction, A Model for Electromagnetic Induction in the Pigeon we observed the maximum induced voltage (15.6 mV) when the Inner Ear magnetic field vector was perpendicular (90) to the plane of As we did not observe an interaction between the presence of the canal and lowest (1.6 mV) when the vector was parallel to light and magnetically induced neuronal activation, our results the plane of the canal (0)(Figure 3B). In contrast, when present- are consistent with a magnetic sensory system based on either ing the control stimulus (with the current running antiparallel magnetite or electromagnetic induction [10]. We have previously through the double-wrapped coils), we did not observe these reported the discovery of an iron-rich organelle in both vestibular characteristic voltage spikes (Figure 3C). Nor did we observe and cochlear hair cells that is associated with vesicular struc- voltage spikes when removing the model of the semicircular ca- tures, but because it is primarily composed of ferrihydrite it lacks nal from the circuit, demonstrating that induction does not occur the magnetic properties to function as the hypothesized torque- in the connecting shielded wires (Figure 3D). based magnetoreceptor [11–13]. Moreover, a systematic screen Next, we measured the dimensions of the semicircular canals for magnetite in the pigeon lagena using synchrotron-based in pigeons drawing on previously generated computed tomogra- X-ray fluorescence microscopy and electron microscopy has phy (CT) scans (n = 3 birds) [18](Figure S1A). This revealed that failed to identify extra- or intracellular magnetite crystals [14]. In the mean loop diameter of the posterior canal was 4.20 ± light of these findings, we focused on electromagnetic induction 0.01 mm, the anterior canal was 6.37 ± 0.05 mm, and the lateral [15]. First proposed by Camille Viguier in 1882, this hypothesis canal was 5.18 ± 0.15 mm (mean ± SD). Drawing on these mea- predicts that as a terrestrial animal moves through the Earth’s surements and the voltage induced in our 21-cm-diameter static magnetic field a voltage is induced within the conductive model, we were able to estimate the electric field generated endolymph of the semicircular canals [4, 16].
Recommended publications
  • Magnetite Biomineralization in the Human Brain (Iron/Extremely Low Frequency Magnetic Fields) JOSEPH L
    Proc. Natl. Acad. Sci. USA Vol. 89, pp. 7683-7687, August 1992 Biophysics Magnetite biomineralization in the human brain (iron/extremely low frequency magnetic fields) JOSEPH L. KIRSCHVINK, ATSUKO KOBAYASHI-KIRSCHVINK, AND BARBARA J. WOODFORD* Division of Geological and Planetary Sciences, The California Institute of Technology, Pasadena, CA 91125 Communicated by Leon T. Silver, May 7, 1992 ABSTRACT Although the mineral magnetite (Fe3O4) is mollusks (12), arthropods (13), and chordates (14, 15) and is precipitated biochemically by bacteria, protists, and a variety suspected in many more groups (16). In the microorganisms of animals, it has not been documented previously in human (10, 11) and fish (15), linear chains of membrane-bound tissue. Using an ultrasensitive superconducting magnetometer crystals of magnetite (magnetosomes) form structures best in a clean-lab environment, we have detected the presence of described as "biological bar magnets." ferromagnetic material in a variety of tissues from the human We report here that human tissues possess similar crystals brain. Magnetic particle extracts from solubilized brain tissues of biogenic magnetite, with minimum estimates between 5 examined with high-resolution transmission electron micros- and 100 million single-domain crystals per gram in the tissues copy, electron diffraction, and elemental analyses identify of the human brain. Magnetic particle extracts from solubi- minerals in the magnetitemaghemite family, with many ofthe lized tissues examined with high-resolution transmission crystal morphologies and structures resembling strongly those electron microscopy (TEM) and electron diffraction identify precipitated by magnetotactic bacteria and fish. These mag- minerals in the magnetite-maghemite solid solution, with netic and high-resolution transmission electron microscopy many crystal morphologies and structures resembling those measurements imply the presence of a minimum of 5 million precipitated by magnetotactic bacteria and fish.
    [Show full text]
  • Sea Turtles: Navigation and Orientation C
    S Sea Turtles: Navigation and Orientation C. M. F. Lohmann and K. J. Lohmann, University of North Carolina, Chapel Hill, NC, USA ã 2010 Elsevier Ltd. All rights reserved. Sea Turtle Life History This reliance on light cues has undoubtedly served sea turtles well over the course of their 120 My history. On Among the sea turtles, orientation and navigation have wilderness beaches, they are seldom misoriented toward been studied most thoroughly in loggerhead (Caretta car- the land. On beaches shared with modern humans, how- etta) and green turtles (Chelonia mydas). These two species ever, artificial lighting has been a serious problem. As have similar life histories and are highly migratory. development overtook the beaches of south Florida in In the typical case, females lay clutches of 100–150 eggs the latter twentieth century, young turtles began crawling and bury them in the sand of the nesting beach. After toward parking lots and tennis courts instead of toward 2 months, the young turtles hatch below ground and the sea. Caught there at sunrise, the turtles often died slowly dig their way to the surface. The hatchlings emerge from predation and desiccation before they could find onto the surface of the sand, then scramble to the sea and their way back to the ocean. Happily, the understanding migrate offshore, where they begin a prolonged period in of their orientation mechanisms has informed conserva- the open sea, sometimes migrating across entire ocean tion efforts throughout the world. In most populated basins. Later, juveniles recruit to various coastal feeding areas, an effort is now made to reduce beach lighting on areas.
    [Show full text]
  • Arxiv:1702.00538V2 [Physics.Bio-Ph] 24 May 2019
    In-vivo biomagnetic characterisation of the American cockroach Ling-Jun Kong,1, 2 Herbert Crepaz,1, 3 Agnieszka G´orecka,1, 4 Aleksandra Urbanek,5 Rainer Dumke,1, 3 and Tomasz Paterek1, 3 1School of Physical and Mathematical Sciences, Nanyang Technological University, 637371 Singapore 2MOE Key Laboratory of Weak Light Nonlinear Photonics and School of Physics, Nankai University, Tianjin 300071, China 3Centre for Quantum Technologies, National University of Singapore, 117543 Singapore 4School of Physics and Astronomy, Monash University, Victoria 3800, Australia 5Department of Invertebrate Zoology and Parasitology, University of Gda´nsk, 80-308 Poland We present a quantitative method, utilising a highly sensitive quantum sensor, that extends ap- plicability of magnetorelaxometry to biological samples at physiological temperature. The observed magnetic fields allow for non-invasive determination of physical properties of magnetic materials and their surrounding environment inside the specimen. The method is applied to American cock- roaches and reveals magnetic deposits with strikingly different behaviour in alive and dead insects. We discuss consequences of this finding to cockroach magneto-reception. To our knowledge, this work represents the first characterisation of the magnetisation dynamics in live insects and helps to connect results from behavioural experiments on insects in magnetic fields with characterisation of magnetic materials in their corpses. I. INTRODUCTION Many species are capable of perceiving the world through senses inaccessible to humans. Polarisation vision of marine species [1] or magnetic field detection by migratory birds [2] being two well-known examples. Magneto- reception is in fact common to a wide range of organisms, ranging from bacteria to higher vertebrates, and has evolved to a fine-tuned sensory system that maybe even takes advantage of quantum coherence [3].
    [Show full text]
  • Magnetite-Based Magnetoreception Joseph L Kirschvink*, Michael M Walker† and Carol E Diebel‡
    462 Magnetite-based magnetoreception Joseph L Kirschvink*, Michael M Walker† and Carol E Diebel‡ Orientation, navigation, and homing are critical traits expressed vision [5]); as we note below, this assumption is unlikely by organisms ranging from bacteria through higher vertebrates. from an evolutionary perspective. The most plausible Sensory systems that aid such behavior have provided key mechanism — that animals might have a built-in ‘compass selective advantages to these groups over the past 4 billion needle’ — was rejected initially on the assumption that years, and are highly evolved; magnetoreception is no animals “had no physiological ferromagnetic materials” exception. Across many species and groups of organisms, [6]. Third and finally, prior to the 1970’s, behavioral evi- compelling evidence exists that the physical basis of this dence for the existence of magnetoreception was difficult response is tiny crystals of single-domain magnetite (Fe3O4). It to reproduce and virtually all laboratory-based attempts to is the opinion of the authors that all magnetic field sensitivity in train animals to discriminate magnetic cues had failed. living organisms, including elasmobranch fishes, is the result of a highly evolved, finely-tuned sensory system based on single- Despite these controversies, the reports of Earth-strength domain, ferromagnetic crystals. magnetic effects on behavior did not die away, and it remained an attractive hypothesis to explain long-distance Addresses animal migration. Because animals are able to navigate *Division
    [Show full text]
  • Animal Magnetism: a Study of Captive Grey Wolves at Rest and Their Orientation Relative to Earth’S Magnetic Field Max Yasgur, John Jay High School
    Yasgur 1 Animal Magnetism: A study of captive grey wolves at rest and their orientation relative to Earth’s magnetic field Max Yasgur, John Jay High School Yasgur 2 Acknowledgements This research was conducted with the help of my mentor, Ms. Rebecca Bose. She aided this research through elucidation of common wolf behavior as well as the possible procedures in captive wolf imaging, which was the primary method of data collection. My mentor also allowed access to observe the wolves. My teacher, Ms. Anne Marie Lipinsky, reviewed my paper and my forms. Yasgur 3 Table of Contents Topics Acknowledgements 2 Abstract 4 Introduction 5 Statement of Purpose 6 Materials & Methods 6 Results 7 Discussion 11 Conclusions & Significance 13 References 13 Tables and Figures Table 1 7 Figure 1 8 Figure 2 9 Figure 3 9 Figure 4 9 Figure 5 9 Figure 6 9 Figure 7 10 Figure 8 10 Table 2 11 Yasgur 4 Abstract The field of magnetoreception studies animals and their sensitivity to Earth’s magnetic field. Over the past 50 years, the roster of magnetically-sensitive animals has grown significantly, but one animal has yet to make the list: the grey wolf (Canis lupus). This study attempts to determine if the captive grey wolf ​ ​ orients along a consistent directional axis during rest. The literature suggests that other higher order mammals with similar physiology show signs of magnetoreceptive behaviors at rest, but little is known about the wolf in this regard. In this study, four captive grey wolves were observed (n = 107 observations) over the course of five weeks using a camera-compass iOS application.
    [Show full text]
  • Eyes Are Essential for Magnetoreception in a Mammal
    bioRxiv preprint doi: https://doi.org/10.1101/2020.05.07.082388; this version posted May 7, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Eyes are essential for magnetoreception in a mammal Kai R. Caspar1, Katrin Moldenhauer1, Regina E. Moritz1,3, E. Pascal Malkemper2, Sabine Begall1,4* 1Department of General Zoology, University of Duisburg-Essen, Universitaetsstr. 5, 45117 Essen, Germany 2Max Planck Research Group Neurobiology of Magnetoreception, Center of Advanced European Studies and Research (CAESAR), Ludwig-Erhard-Allee 2, 53175 Bonn, Germany 3Department Vision, Visual Impairment & Blindness, Faculty 13, Technical University of Dortmund, Emil-Figge-Straße 50, 44227 Dortmund, Germany 4Department of Game Management and Wildlife Biology, Faculty of Forestry and Wood Sci- ences, Czech University of Life Sciences, 16521 Praha 6, Czech Republic Correspondence to [email protected] Abstract: Several groups of mammals use the Earth’s magnetic field for orientation, but their magnetosensory organ remains unknown. The Ansell’s mole-rat (Fukomys anselli) is a subterranean rodent with innate magnetic orientation behavior. Previous studies proposed that its magnetoreceptors are located in the eye. To test this hypothesis, we assessed magnetic orientation in enucleated mole-rats. Initially, we demonstrate that enucleation of mole-rats does not lead to changes in routine behaviors. We then studied magnetic compass orientation by employing a well-established nest building assay. To ensure that directional responses were based on magnetic parameters, we tested animals under four magnetic field alignments.
    [Show full text]
  • Genomic Expansion of Magnetotactic Bacteria Reveals an Early Common Origin of Magnetotaxis with Lineage-Specific Evolution
    The ISME Journal (2018) 12:1508–1519 https://doi.org/10.1038/s41396-018-0098-9 ARTICLE Genomic expansion of magnetotactic bacteria reveals an early common origin of magnetotaxis with lineage-specific evolution 1,2,3 1,2,3,4 5 5 1,2,6 Wei Lin ● Wensi Zhang ● Xiang Zhao ● Andrew P. Roberts ● Greig A. Paterson ● 7 1,2,3,4 Dennis A. Bazylinski ● Yongxin Pan Received: 4 October 2017 / Revised: 23 February 2018 / Accepted: 26 February 2018 / Published online: 26 March 2018 © The Author(s) 2018. This article is published with open access Abstract The origin and evolution of magnetoreception, which in diverse prokaryotes and protozoa is known as magnetotaxis and enables these microorganisms to detect Earth’smagneticfield for orientation and navigation, is not well understood in evolutionary biology. The only known prokaryotes capable of sensing the geomagnetic field are magnetotactic bacteria (MTB), motile microorganisms that biomineralize intracellular, membrane-bounded magnetic single-domain crystals of either magnetite (Fe3O4)orgreigite(Fe3S4) called magnetosomes. Magnetosomes are responsible for magnetotaxis in MTB. Here we report the first large-scale metagenomic survey of MTB from both northern and southern hemispheres combined with 28 1234567890();,: genomes from uncultivated MTB. These genomes expand greatly the coverage of MTB in the Proteobacteria, Nitrospirae,and Omnitrophica phyla, and provide the first genomic evidence of MTB belonging to the Zetaproteobacteria and “Candidatus Lambdaproteobacteria” classes. The gene content and organization of magnetosome gene clusters, which are physically grouped genes that encode proteins for magnetosome biosynthesis and organization, are more conserved within phylogenetically similar groups than between different taxonomic lineages.
    [Show full text]
  • Magnetotactic Bacteria: Isolation, Imaging, and Biomineralization
    Magnetotactic Bacteria: Isolation, Imaging, and Biomineralization Dissertation Presented in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in the Graduate School of The Ohio State University By Zachery Walter John Oestreicher Graduate Program in Geological Sciences. The Ohio State University 2012 Committee: Steven K. Lower, Advisor Wendy Panero Olli Tuovinen Brian H. Lower Copyright by Zachery Walter John Oestreicher 2012 Abstract Magnetotactic bacteria (MTB) are a specialized group of bacteria that produce very small magnets inside their cells. There are a number of reasons that I decided to study these particular microorganisms. MTB are universally found in aquatic environments and they can be isolated with a simple magnet. These bacteria have the distinct ability to synthesize nanometer-scale crystals of magnetite (Fe3O4) or greigite (Fe3S4) inside their cells. This type of biomineralization serves as a model for mineral formation in more complex organisms such as birds, bees, and fish. The magnetite from MTB can be used as a biomarker, called magnetofossils, for past life on earth as well as possible extraterrestrial life forms (e.g., putative magnetofossils in Martian meteorites such as the Allan Hills meteorite). Magnetofossils are novel biomarkers because the magnetite from MTB has a specific crystal shape, narrow size range, and flawless chemical composition, which make them easily identified as biological origin. These same crystallographic attributes could also be exploited in biomimicry. For example, in vitro synthesis of magnetic crystals could have applications in medicine, electronic storage devices, and even environmental remediation. The work in this dissertation touches on all of these concepts.
    [Show full text]
  • Magnetite Biomineralization and Geomagnetic Sensitivity in Higher Animals: an Update and Recommendations for Future Study
    Bioelectromagnetics 10:23%259 (1989) Invited Paper Magnetite Biomineralization and Geomagnetic Sensitivity in Higher Animals: An Update and Recommendations for Future Study Joseph L. Kirschvink Division of Geological and Planetary Sciences, The California Institute of Technology, Pasadena Magnetite, the only known biogenic material with ferromagnetic properties, has been identified as a biochemical precipitate in three of the five kingdoms of living organisms, with a fossil record that now extends back nearly 2 billion years. In the magnetotactic bacteria, protoctists, and fish, single-domain crystals of magnetite are arranged in membrane-bound linear structures called magnetosomes, which function as biological bar magnets. Magnetosomes in all three of these groups bear an overall structural similarity to each other, which includes alignment of the individual crystallographic [ 11 I] directions parallel to the long axis. Although the magnetosomes represent only a small volume fraction in higher organisms, enough of these highly energetic structures are present to provide sensitivity to extremely small fluctuations and gradients in the background geomagnetic field. Previous experiments with elasmobranch fish are reexamined to test the hypothesis that gradients played a role in their successful geomagnetic conditioning, and a variety of four-turn coil designs are considered that could be used to test the various hypotheses proposed for them. Key words: biogenic magnetite, magnetoreception, cetaceans, elasmobranchs, coil designs Received for review September 8, 1988; revision received January 27, 1989. Address reprint requests to Joseph L. Kirschvink, Division of Geological and Planetary Sciences, The California Institute of Technology, Pasadena, CA 91 125. 0 1989 Alan R. Liss, Inc. 240 Kirschvink INTRODUCTION Geomagnetic Sensitivity in Animals Once considered highly unlikely, behavioral evidence now suggests that a variety of living organisms respond to the geomagnetic field.
    [Show full text]
  • Chemical Magnetoreception in Birds: the Radical Pair Mechanism
    PERSPECTIVE Chemical magnetoreception in birds: The radical pair mechanism Christopher T. Rodgersa,b and P. J. Horea,1 aDepartment of Chemistry, Physical and Theoretical Chemistry Laboratory, University of Oxford, South Parks Road, Oxford, OX1 3QZ, United Kingdom; and bOxford Centre for Clinical Magnetic Resonance Research, Level 0, John Radcliffe Hospital, Oxford, OX3 9DU, United Kingdom Edited by Nicholas J. Turro, Columbia University, New York, NY, and approved December 2, 2008 (received for review September 24, 2008) Migratory birds travel vast distances each year, finding their way by various means, including a remarkable ability to perceive the Earth’s magnetic field. Although it has been known for 40 years that birds possess a magnetic compass, avian magnetoreception is poorly understood at all levels from the primary biophysical detection events, signal transduction pathways and neurophysiology, to the processing of information in the brain. It has been proposed that the primary detector is a specialized ocular photoreceptor that plays host to magnetically sensitive photochemical reactions having radical pairs as fleeting intermediates. Here, we present a physi- cal chemist’s perspective on the ‘‘radical pair mechanism’’ of compass magnetoreception in birds. We outline the essential chemical requirements for detecting the direction of an Earth-strength Ϸ50 ␮T magnetic field and comment on the likelihood that these might be satisfied in a biologically plausible receptor. Our survey concludes with a discussion of cryptochrome, the photoactive protein that has been put forward as the magnetoreceptor molecule. ould a chemical reaction be The radical pair mechanism [and a pair model, or to comment on (neuro)- used to detect the direction of few rare variants (10)] is currently the physiological aspects of magnetorecep- the Earth’s magnetic field? At only plausible way in which weak mag- tion, all of which have been covered first sight, most physical chem- netic fields can affect chemical reactiv- authoritatively and extensively in recent Cists would be skeptical.
    [Show full text]
  • Magnetoreception in Microorganisms Caroline Monteil, Christopher Lefèvre
    Magnetoreception in Microorganisms Caroline Monteil, Christopher Lefèvre To cite this version: Caroline Monteil, Christopher Lefèvre. Magnetoreception in Microorganisms. Trends in Microbiology, Elsevier, 2019, 28 (4), pp.266-275. 10.1016/j.tim.2019.10.012. cea-02378779 HAL Id: cea-02378779 https://hal-cea.archives-ouvertes.fr/cea-02378779 Submitted on 7 Nov 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. 1 Magnetoreception in microorganisms 2 3 4 Caroline L. Monteil & Christopher T. Lefevre* 5 6 7 8 Aix-Marseille University, CNRS, CEA, UMR7265 Institute of Biosciences and 9 Biotechnologies of Aix-Marseille, Saint-Paul-lez-Durance, France 10 11 12 13 14 15 16 17 18 19 *Correspondence: [email protected] (C.T. Lefevre). 20 21 Keywords : magnetoreception; biomineralization; magnetosomes; magnetotactic bacteria; 22 protists; holobionts; symbiosis; grazing 1 23 Magnetoreception is the sense whereby organisms geolocate and navigate in response to 24 the Earth’s magnetic field lines. For decades, magnetotactic bacteria have been the only 25 known magnetoreceptive microorganisms. The magnetotactic behaviour of these aquatic 26 prokaryotes is due to the biomineralization of magnetic crystals. While an old report 27 alleged microbial algae with a similar behaviour, recent discoveries have demonstrated 28 the existence of unicellular eukaryotes able to sense the geomagnetic field and revealed 29 different mechanisms and strategies involved in such a sensing.
    [Show full text]
  • Magnetoreception and Its Neural Basis in Spiny Lobsters
    MAGNETORECEPTION AND ITS NEURAL BASIS IN SPINY LOBSTERS David A. Ernst A dissertation submitted to the faculty of the University of North Carolina at Chapel Hill in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Department of Biology (Evolution, Ecology, and Organismal Biology). Chapel Hill 2018 Approved by: Kenneth J. Lohmann Sönke Johnsen William M. Kier Karin S. Pfennig Catherine M. F. Lohmann © 2018 David A. Ernst ALL RIGHTS RESERVED ii ABSTRACT David A. Ernst: Magnetoreception and Its Neural Basis in Spiny Lobsters (Under the direction of Kenneth J. Lohmann) The research presented here investigates magnetoreception (the ability to detect Earth’s magnetic field) and its underlying mechanisms in the Caribbean spiny lobster, Panulirus argus. Spiny lobsters are the only invertebrates known to detect and use directional and positional information from Earth’s magnetic field. Despite decades of research, we still do not know how lobsters, or indeed any animals, are able to perceive magnetic fields. To shed light on this elusive sensory modality, I examine the behavioral and transcriptomic responses of lobsters to strong magnetic stimuli. Behavioral studies revealed that lobsters actively avoid dens with a strong magnetic anomaly and that lobster size is a predictor of avoidance behavior. On average, lobsters that chose dens with the anomaly were significantly smaller than those that chose dens with a non-magnetic weight. These findings are consistent with magnetoreception in lobsters, suggest ontogenetic variation in the lobster’s response to magnetic fields, and indicate that magnetic anomalies might affect the movements of lobsters and other animals in the natural environment.
    [Show full text]